Everyday Taxi Drivers: Do Better Navigators Have Larger Hippocampi? RUNNING TITLE: EVERYDAY TAXI DRIVERS
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bioRxiv preprint doi: https://doi.org/10.1101/431155; this version posted January 2, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Title: Everyday taxi drivers: Do better navigators have larger hippocampi? RUNNING TITLE: EVERYDAY TAXI DRIVERS Steven M. Weisberga, Nora S. Newcombeb, & Anjan Chatterjeec aUniversity of Pennsylvania, bTemple University Steven M. Weisberg ([email protected]), Anjan Chatterjee ([email protected]), Department of Neurology, University of Pennsylvania, Philadelphia, PA 19104. Nora S. Newcombe ([email protected]), Department of Psychology, Temple University, Philadelphia, PA 19122. Declarations of interest: none Correspondence concerning this article should be addressed to Steven M. Weisberg, at Center for Cognitive Neuroscience, University of Pennsylvania, Philadelphia, PA 19104 USA. Email: [email protected]. Phone: 610-212-3113. bioRxiv preprint doi: https://doi.org/10.1101/431155; this version posted January 2, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. EVERYDAY TAXI DRIVERS 1 Abstract Work with non-human animals and human navigation experts (London taxi drivers) suggests that the size of the hippocampus, particularly the right posterior hippocampus in humans, relates to navigation expertise. Similar observations, sometimes implicating other sections of the hippocampus, have been made for aging populations and for people with neurodegenerative diseases that affect the hippocampus. These data support the hypothesis that hippocampal volume relates to navigation ability. However, the support for this hypothesis is mixed in healthy, young adults, who range widely in their navigation ability. Here, we administered a naturalistic navigation task that measures cognitive map accuracy to a sample of 90 healthy, young adults who also had MRI scans. Using a sequential analysis design with a registered analysis plan, we did not find that navigation ability related to hippocampal volume (total, right only, right posterior only). We conclude that navigation ability in a typical population does not correlate with variations in hippocampal size, and consider possible explanations for this null result. Keywords: hippocampus, human behavior, spatial cognition, spatial navigation, structural MRI Abbreviations: ASHS – Automatic Segmentation of Hippocampal Subfields BF – Bayes Factor ERC – Entorhinal cortex MRT – Mental rotation test OSF – Open Science Framework PHC – Parahippocampal cortex SAQ – Spatial anxiety questionnaire SBSOD – Santa Barbara sense of direction scale WRAT-4 – Wide range achievement test 4 – verbal bioRxiv preprint doi: https://doi.org/10.1101/431155; this version posted January 2, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. EVERYDAY TAXI DRIVERS 2 1. Introduction Spatial navigation is a fundamental problem faced by any mobile organism. This ability is supported in part by the hippocampus, which is theorized to construct a cognitive map – knowledge of the distances and directions between landmarks (O’Keefe & Nadel, 1978; Tolman, 1948). Evidence for the role of the hippocampus in navigation comes from functional neural data across a wide range of levels of analysis. At the single-cell level, place cells in the hippocampus fire when an animal is in a certain location (Ekstrom et al., 2003; O’Keefe & Nadel, 1978). At the voxel level, fMRI reveals that the patterns of voxels in the hippocampus map to information about spatial distance (Vass & Epstein, 2013). At the whole hippocampus anatomic level, fMRI reveals that the hippocampus is more active during active navigation than passive travel or when following a familiar route (e.g., Hartley et al. 2003). So, neuronal activity in the hippocampus is consistent with the hypothesis that the hippocampus constructs a cognitive map. Intriguingly, there is reason to suppose that variations in the structure and function of hippocampus may relate to variations in navigation abilities. Maguire and colleagues (2000; 2006) showed that the right posterior hippocampus was enlarged in taxi drivers from London, who memorize an enormous catalog of spatial information and navigate easily around the complex layout of London. Further work showed that elderly taxi drivers who were still driving taxis had enlarged right posterior hippocampi compared to elderly taxi drivers who had stopped (Woollett, Spiers, & Maguire, 2009). Although this work on taxi drivers presented among the first data to show a correlation between hippocampal volume and aspects of navigation behavior, the sample sizes were small (less than 20 participants in most studies). And despite making claims about increased right posterior hippocampal volume and decreased right anterior hippocampal volume in taxi drivers, the researchers did not test the key interaction between bioRxiv preprint doi: https://doi.org/10.1101/431155; this version posted January 2, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. EVERYDAY TAXI DRIVERS 3 posterior and anterior hippocampal volume between taxi drivers and controls, rendering this conclusion unsupported by the data. Nevertheless, complementary research in non-human animals has supported the notion that larger hippocampi are associated with better navigation (Sherry, Jacobs, & Gaulin, 1992). Importantly, changes in hippocampal size may occur within an animal’s lifespan. Male meadow voles, for example, show cell proliferation in the dentate gyrus concomitant with hippocampal volume increases in the breeding season (when males have greater spatial navigation requirements) compared to the non-breeding season (Galea & McEwen, 1999). Similarly, compromise of the hippocampus is associated with spatial navigation deficits. Poor spatial navigation occurs in patients with Alzheimer’s disease (Deipolyi, Rankin, Mucke, Miller, & Gorno-Tempini, 2007; Konishi et al., 2018; Moodley et al., 2015; Plancher, Tirard, Gyselinck, Nicolas, & Piolino, 2012), patients with brain lesions (Kolarik, Baer, Shahlaie, Yonelinas, & Ekstrom, 2018; Rosenbaum et al., 2000; Smith & Milner, 1981) and in the elderly (Konishi, Mckenzie, Etcharnendy, Roy, & Bohbot, 2017; Moodley et al., 2015). These groups show reduced hippocampal volume, suggesting that a healthy hippocampus is critical for normal spatial navigation function. Collectively, this body of literature seems to make a powerful case for an association between hippocampal volume and navigation. However, evidence from healthy young adults is more mixed. Some research studies are positive. First, there are findings that hippocampal volume correlates with specific navigationally-relevant spatial tasks, notably perspective taking. (in which an unseen view must be imagined). Perspective taking correlates with spatial memory for large-scale environments (Weisberg & Newcombe, 2016) and elicits neural activation in the hippocampus (Lambrey, Doeller, Berthoz, & Burgess, 2012). Hartley and Harlow (2012) created a perspective-taking task in which participants match an image of three-dimensional mountains bioRxiv preprint doi: https://doi.org/10.1101/431155; this version posted January 2, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. EVERYDAY TAXI DRIVERS 4 to an image of the same mountains range viewed from a different perspective while ignoring similar-looking foils. Accuracy on this task correlated with bilateral hippocampal volume. Sherrill and colleagues (2018) measured participant’s ability to find a goal from first-person and map perspectives after viewing a map with their position and the position of the goal. Accuracy in the first-person condition correlated with bilateral posterior hippocampal volume. Second, hippocampal volume correlates with specific strategies used by healthy young adults when navigating. Bohbot and colleagues measured spatial navigation strategy using a task in which the direction to goals could be based on which response should be made (e.g., to one’s right; thought to rely on the caudate nucleus), or based on each goal’s position relative to external landmarks (e.g., the church is to the right of the school; thought to rely on the hippocampus), independent of success at finding a goal. They found large positive correlations with hippocampal volume and the number of goals found relative to external landmarks (Bohbot, Lerch, Thorndycraft, Iaria, & Zijdenbos, 2007). Third, using a self-report measure of navigation ability, two studies with large samples reported correlations with hippocampal volume, although the effect sizes were modest (Hao et al., 2016; Wegman et al., 2014). None of these approaches is direct, however. Perspective